(MIS 4) Arctic Ground Squirrel Middens and a Squirrel-Eye-View of the Mammoth-Steppe

Quaternary Science Reviews 30 (2011) 2220e2237

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Early Wisconsinan (MIS 4) Arctic ground squirrel middens and a squirrel-eye-view of the mammoth-steppe

Grant D. Zazula a,*, Duane G. Froese b, Scott A. Elias c, Svetlana Kuzmina b, Rolf W. Mathewes d a Yukon Palaeontology Program, Department of Tourism & Culture, Government of Yukon, Box 2703 L2-A, Whitehorse, Yukon, Canada Y1A 2C6 b Department of Earth and Atmospheric Sciences, University of Alberta, 1-26 Earth Sciences Building, Edmonton, Alberta, Canada T6G 2E3 c Geography Department, Royal Holloway, University of London, Egham, Surrey TW200EX, United Kingdom d Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada V5A 1S6 article info abstract

Article history: Fossil arctic ground squirrel (Spermophilus parryii) middens were recovered from ice-rich loess sedi- Received 24 June 2009 ments in association with Sheep Creek-Klondike and Dominion Creek tephras (ca 80 ka) exposed in west- Received in revised form central Yukon. These middens provide plant and insect macrofossil evidence for a steppe-tundra 8 January 2010 ecosystem during the Early Wisconsinan (MIS 4) glacial interval. Midden plant and insect macrofossil Accepted 21 April 2010 data are compared with those previously published for Late Wisconsinan middens dating to Available online 23 May 2010 w25e2914C ka BP (MIS 3/2) from the region. Although multivariate statistical comparisons suggest differences between the relative abundances of plant macrofossils, the co-occurrence of steppe-tundra plants and insects (e.g., Elymus trachycaulus, Kobresia myosuroides, Artemisia frigida, Phlox hoodii, Con- natichela artemisiae) provides evidence for successive reestablishment of the zonal steppe-tundra habitats during cold stages of the Late Pleistocene. Arctic ground squirrels were well adapted to the cold, arid climates, steppe-tundra vegetation and well-drained loessal soils that characterize cold stages of Late Pleistocene Beringia. These glacial conditions enabled arctic ground squirrel populations to expand their range to the interior regions of Alaska and Yukon, including the Klondike, where they are absent today. Arctic ground squirrels have endured numerous Quaternary climate oscillations by retracting populations to disjunct “interglacial refugia” during warm interglacial periods (e.g., south-facing steppe slopes, well-drained arctic and alpine tundra areas) and expanding their distribution across the mammoth-steppe biome during cold, arid glacial intervals. Crown Copyright Ó 2010 Published by Elsevier Ltd. All rights reserved.

1. Introduction terrestrial ecosystems for much of the Quaternary prior to the Last Glacial Maximum (LGM) or ecological responses to climate change The hallmark characteristic of Quaternary environmental change over successive glacialeinterglacial cycles. In reconstructing envi- is the cyclical oscillation between warm interglacial and cold glacial ronmental change over glacialeinterglacial time scales, it is impor- climate intervals, largely driven by orbital perturbations and their tant to recognize that for approximately 80% of the Quaternary, effects on solar insolation. Evidence for these climate ﬂuctuations is global climates were colder than the present interglacial (Ehlers and recorded in d18O and other proxy data from deep sea marine sedi- Gibbard, 2004). As such, for many present-day organisms, in the ments (Martinson et al., 1987; Shackleton, 1987) and cores taken circumpolar region, glacial conditions, or at least conditions char- from the Greenland (Dansgaard et al., 1993) and Antarctic (EPICA, acterized by colder than present climates, can be considered to 2004) ice caps. However, long Quaternary terrestrial paleoecolog- represent the “norm” in terms of their typical ecological adaptations ical records are rare, especially in the northern hemisphere where (Rull, 2009). continental glacial advances have effectively removed much of the Unlike most of northern North America, vast areas of Alaska and sedimentary archive from previous intervals. Thus, there is limited adjacent Yukon (Eastern Beringia) escaped glaciation, and this understanding of the composition or function of high latitude region contains a terrestrial sedimentary archive that spans much of the Late Cenozoic (Hopkins et al., 1982; Froese et al., 2009). Since many of these deposits are older than the effective limits of w 14 * Corresponding author. Fax: þ1 867 667 5377. radiocarbon dating ( 50 000 C yr BP), development of a detailed E-mail address: [email protected] (G.D. Zazula). geochronology for this region has relied on other methods. In

0277-3791/$ e see front matter Crown Copyright Ó 2010 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.quascirev.2010.04.019 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2221 particular, much of Eastern Beringia is in the fall-out zone of distal Knowledge about Beringian biota from multiple intervals can help tephra from the Aleutian and WrangelleSt. Elias volcanic fields us understand the nature of northern biotic refugia and address (Preece et al., 1999, 2000; Begét, 2001; Westgate et al., 2008). how these ecosystems and organisms respond to climate change Tephra can be dated with direct (i.e. fission track, Westgate, 1989) over glacial-interglacial time scales. and indirect (i.e. luminscence or from associated radiocarbon ages, In this paper, we present plant and insect macrofossil data from Berger et al., 1996; Froese et al., 2002; Demuro et al., 2008) methods 64 fossil arctic ground squirrel (Spermophilus parryii) middens and correlated regionally by geochemical analyses. At least 70 (nests and caches) recovered in association with SCt-K/DCt (early tephras have been identified in Eastern Beringia thus far and have MIS 4 marker beds, ca 80 ka) from ice-rich loess exposures in the facilitated the study of regional Late Cenozoic environmental Klondike goldfields of west-central Yukon (Fig. 1). Pleistocene arctic change (Westgate et al., 1990; Begét, 2001; Westgate et al., 2005). ground squirrel middens have been recognized and examined from Frozen “muck” sediments are commonly exposed by placer gold Siberia (Gubin et al., 2001, 2003; Zanina, 2005), Alaska (Guthrie, mining in valleys of central Alaska and Yukon, yielding a wealth of 1990) and Yukon (Harington, 1984, 2003; Zazula et al., 2005, Pleistocene fossil biota (Guthrie, 1990; Péwé et al., 1997; Harington, 2006a, 2007) and consist of frozen amalgamations of plants 2003; Zazula et al., 2005, 2007). Muck consists of perennially remains that include both graminoid vegetative materials used by frozen, unconsolidated, organic-rich loess found commonly along arctic ground squirrels for nests, and seeds and fruits that were north and north-easterly facing sites and in the bottoms of narrow cached over the winter (Zazula, et al., 2005, 2006b). Plant and other valleys (Fraser and Burn, 1997; Kotler and Burn, 2000; Froese et al., biotic remains from the middens provide detailed, local paleoeco- 2009). Throughout the summer, new exposures of muck are logical records because present-day arctic ground squirrels are constantly created through natural melting and placer mining. known to forage in a relatively limited radius from their nests In the ice-rich loessal deposits of the Klondike goldfields in west- (Batzli and Sobaski, 1980; Zazula et al., 2006b). Although the central Yukon, Dawson tephra (Dt), dating to w25 30014CyrBP paleoecological data from midden samples are certainly biased (w30 000 cal. yr BP) serves as a stratigraphic marker for the onset towards preferred cache forage and nest building plant taxa (Zazula glacial conditions at the Marine Isotope Stage (MIS) 3/2 transition et al., 2006b), the wide range of species represented in previously (Froese et al., 2002, 2006, 2009; Zazula et al., 2006a), while Sheep analyzed fossil samples suggest that they adequately represent Creek tephra-Klondike (SCt-K) and Dominion Creek tephra (DCt), overall local plant community composition (Zazula et al., 2005, dating to 82 9 ka, mark the onset of the Early Wisconsinan glacial 2007). These midden data are compared with those from 48 interval of MIS 4 (Westgate et al., 2005, 2008). Reconstructing fossil middens which date to the Late Wisconsinan glacial interval paleoenvironments associated with these tephras has been the (MIS 3/2 transition) w25 and 29 ka14CyrBP(Zazula et al., 2007). focus of interdisciplinary research (Sanborn et al., 2006; Zazula Comparison of the Late Wisconsinan (MIS 3/2 transition) and Early et al., 2006a). Paleoenvironmental records for early MIS 2 (Late Wisconsinan (MIS 4) middens are used to examine vegetation, Wisconsinan) from the Klondike include fossil arctic ground squirrel arctic ground squirrel adaptations and the ecology of mammoth- middens (Zazula et al., 2005, 2007), peat and in situ vegetation steppe biome during two successive glacial intervals. (Zazula et al., 2003, 2006a; Froese et al., 2006) and loessal paleosols (Sanborn et al., 2006). Together, these data provide evidence for 2. Methods zonal cryoxerophilous steppe-tundra vegetation that occupied well-drained loessal soils during the onset of the last major Pleis- Fossil arctic ground squirrel middens (Figs. 2 and 3)were tocene cold stage. collected at exposures of Pleistocene ice-rich silt along Dominion Although many of the paleoecological details are becoming Creek (n ¼ 38), Quartz Creek (n ¼ 17), and Irish Gulch (n ¼ 9) (Fig. 1) established for Eastern Beringia during the last glaciation (Elias during several visits through the summers of 2002e2005. Labo- et al., 1997; Goetcheus and Birks, 2001; Guthrie, 2001; Ager, ratory methods for midden macrofossil analysis follow Zazula 2003; Bigelow et al., 2003; Zazula et al., 2005, 2007) many ques- (2006). Middens were immersed in water to disaggregate the tions remain about paleoenvironments during earlier glacial plant material before sorting under a dissecting microscope. Plant intervals. A prevailing interpretation of this glacial environment remains were identified to the most precise taxonomic resolution has been termed the “mammoth-steppe” (Guthrie 1990, 2001). The possible. Identification of plant material was conducted by mammoth-steppe model as put forth by Guthrie (1990, 2001) is comparison with herbarium reference specimens from the based on two lines of fossil evidence: 1) the dominance of grass University of Alberta, University of British Columbia, University of (Poaceae), sedge (Cyperaceae), sagebrush (Artemisia) and various Alaska, Fairbanks, Simon Fraser University and Yukon Palae- forbs in regional MIS 2 pollen data, and 2) the dominance of large ontology Program. Vascular plant nomenclature follows the Flora of mammal grazers in regional Late Pleistocene fossil vertebrate North America (Flora of North America Editorial Committee, 1993). faunas, including woolly mammoths (Mammuthus primigenius), Inferred habitat data follows Cody (2000) and some ecological and horses (Equus spp.), and steppe-bison (Bison priscus). Together, the biogeographic information was obtained from Hultèn (1937, 1968). reconstructed regional ecosystem characterized by high latitude Individual plant taxa from each midden were quantified using grasslands, or “steppe-tundra” and the associated large mammal a relative abundance index (RAI) where 0 ¼ absent, 1 ¼ <1%, grazing community, can be summarized as the mammoth-steppe. 2 ¼ 1e5%, 3 ¼ 6e25%, 4 ¼ 26e50%, 5 ¼ 51e75% and 6 ¼ >75% of the Guthrie (1990, 2001) suggests the broadscale uniformity of both entire midden contents (Zazula, 2006, 2007). The majority of plant pollen and vertebrate data from across the Holarctic, indicates the material in each midden was assigned the “miscellaneous vegeta- mammoth-steppe biome stretched from England to Yukon during tion” category which includes graminoid and other unidentified the last glaciation. Further, Guthrie (1990, 2001) has suggested that herbaceous foliage and stems presumably used by the squirrels as the holarctic mammoth-steppe biome responded synchronously nesting material. Since the interval distance within each RAI is not with northern hemisphere climate fluctuations, with xerophilous uniform, mid-point values for each RAI class interval were used for steppe-tundra vegetation and the mammoth-fauna expanding quantitative analyses (RAI mid-point values: 0 ¼ 0, 1 ¼ 0.5%, 2 ¼ 3%, across the unglaciated regions of Eurasia and northern North 3 ¼ 16%, 4 ¼ 38%, 5 ¼ 63% and 6 ¼ 88%). Mid-points are useful America during successive Quaternary cold stages. However, approximations for RAI or other ecological class data when the detailed, multi-proxy paleoecological records from multiple cold exact abundance value for each taxon is not measured (e.g. Mitchell stages in Beringia are not available to test this hypothesis. et al., 1988; Peck et al., 2004). Mean RAI mid-points based on all 64 2222 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Fig. 1. Map of Alaska and Yukon Territory with Klondike area inset showing locations of study sites in Klondike goldﬁelds.

middens were calculated to estimate each taxon’s overall abun- (Kenkel and Orlóci, 1986; Clarke, 1993; McCune and Grace, 2002; dance. RAI values of zero (RAI ¼ 0) were included in the mean Lamb et al., 2003). Samples and species are plotted along n ordi- calculation. nation axes as defined by the optimal solution using the Sørensen’s Insects from the middens were picked during midden sorting by (Bray-Curtis) similarity distance (McCune and Grace, 2002). In the G. Zazula and later identified by S. Kuzmina and S. Elias. Ground and NMS solution, each taxon is assigned an r2 value which reflects the rove beetles were used to obtain estimates of seasonal temperature amount of variance in the overall dataset which can be accounted using the Mutual Climatic Range (MCR) method based on estimates for by that taxon. Difference in plant macrofossil assemblages of seasonal the species climate envelopes (Elias, 2000). Tempera- between MIS 3/2 and MIS 4 was tested using a Multiple Response tures presented are uncalibrated MCR estimates based on total Permutation Procedure (MRPP) with the Sørensen’s distance climate envelopes of present-day taxa. measure (Zimmerman et al., 1985). MRPP is a non-parametric Multivariate analyses were conducted to compare the Early analogue of Discriminant Function Analysis (DFA), which supports Wisconsinan midden data with those previously published of Late a multivariate test of the null hypothesis of no significant difference Wisconsinan age (Zazula et al., 2007). For numerical analyses, the between a priori groups of samples (Williams, 1983; McCune and miscellaneous vegetation class (graminoid and other nesting Grace, 2002). In the MRPP, and A statistic measured the grouping material) was removed from the data matrix. A KruskaleWallis test “effect size”, or distinctiveness of groups, on a scale of 0e1. Values available in JMP 5.01 (Sall et al., 2001) confirmed there were no of A > 0.3 are considered fairly high. Indicator Species Analysis (ISA) significant differences in mean nesting material abundance from was used to identify species that were significantly more frequent the MIS 3/2 and MIS 4 midden samples (P ¼ 0.5887). The resultant and abundant in middens of either the MIS 3/2 or MIS 4 intervals. data matrix was relativized by sample sum of squares (McCune and The indicator values are calculated by multiplying the relative Grace, 2002) to standardize the amount of cache material (seeds abundance of each taxon in a particular group by the relative and fruits) in each midden sample and ensure comparison of frequency of the species’ occurrence in that group (Dufrêne and relatively equal sample sizes. An arcsine square root transformation Legendre, 1997; McCune and Grace, 2002). was applied to these data. This transformation is appropriate for ecological data matrices based on proportional data with abundant 3. Results zeros and is recommended to improve normality (McCune and Grace, 2002). 3.1. MIS 4 loess and paleosol stratigraphy of the Klondike All multivariate tests were conducted with PC-Ord 4.14 (McCune and Mefford, 1999). The overall trends and structure in the midden Fossil middens and loessal paleosols are commonly observed in plant macrofossil data were explored using Non-Metric Multidi- the Klondike within ice-rich sediments in association with SCt-K mensional Scaling (NMS) using the autopilot program with the and DCt (Fig. 4). (Westgate et al., 2005, 2008; Sanborn et al., 2006; slow and thorough analysis option and the default settings in PC- Froese et al., in preparation). DCt has a glass fission track age of Ord 4.14 (McCune and Mefford, 1999). NMS is a non-parametric 82 9 ka and occurs stratigraphically above and in close associa- ordination method well suited to non-normally distributed tion with SCt-K. Optically Stimulated Luminescence (OSL) ages ecological data that avoids many of the assumptions about under- obtained from sediments associated with SCt-K are consistent with lying structures of data made by traditional ordination methods the glass FT age on the DCt (Westgate et al., 2005, 2008). Both G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2223

Fig. 2. Various arctic ground squirrel remains from MIS 4 sediments. a) four middens above Sheep Creek tephra e Klondike at Dominion Creek site; b) close up of frozen midden from previous photo with knife handle (9.0 cm long) for scale; c) midden with arctic ground squirrel skull at Dominion Creek site (knife handle is 10.0 cm long); d) arctic ground squirrel midden in MIS 4 loess at Quartz Creek (black knife handle is 9.0 cm long); e) fruit/seed cache associated with Sheep Creek tephra e Klondike at Dominion Creek site (knife handle is 9.0 cm long); f) squirrel tunnel in MIS 4 loess at Quartz Creek. tephras occur stratigraphically above fossil forest beds and organic- wedges that are 1e2 m in width disrupt the two lowermost loessal rich deposits correlated with the ﬁnal substage of the last inter- soils, but do not extend as far stratigraphically as Soil 1. Soil 1 glacial, likely MIS 5a (Westgate et al., 2005, 2008; Froese et al., in probably formed under loess accretion in more xeric conditions than preparation). Based on this chronology, loessal paleosols and Soil 2 or 3 and is most similar to MIS 2 paleosols associated with arctic ground squirrel middens associated with these tephra Dawson tephra (Sanborn et al., 2006). At Dominion Creek and at an correlate with the onset of glacial conditions during early MIS 4 additional site at nearby Whitman Creek (Froese et al., 2003), sand (Early Wisconsinan). Two middens recovered stratigraphically wedges and sandsheets cap the MIS 4 loess-paleosol sequence. above SCt-K at Quartz Creek date to >42 00014C yr BP (Beta e Taken together, tephra, loess sediments and paleosols at these sites 202422; Beta e 203420) and are consistent with an MIS 4 age. record increasing aridity during the transition from late MIS 5a Within the MIS 4 loess deposits at Dominion Creek and Quartz through MIS 4. However, soil active layers must have been thicker creek, paleosols and other stratigraphic features provide information and better drained than modern throughout the loess/paleosol on substrates and environmental conditions associated with arctic sequence as evidenced by the abundance of fossil ground squirrel ground squirrel middens. Three distinct paleosols occur within the middens (Sanborn et al., 2006; Zazula et al., 2007). loess (Fig. 4; Sanborn et al., 2006). Pedological characteristics suggest more mesic conditions with substantial cryoturbation in the 3.2. Midden plant macrofossils lowermost Soils 2 and 3 (Fig. 4), with generally decreasing moisture stratigraphically upwards and limited cryoturbation in the upper Plant remains from the middens are dominated by miscella- part of the sequence (Soil 1 and above). At Dominion Creek, ice- neous vegetative material that includes graminoid foliage nesting 2224 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Erysimum cf. cheiranthoides type (43.8%; 11.63; 6). Some taxa were recovered frequently, but in low abundance such as Ranunculus eschscholtzii-sulphureus type (45.3%; 1.06; 3) and Elymus sp. (43.8%, 0.41; 2). Some rare taxa were only recovered from one (Juncus sp., Saxifraga sp., Astragalus alpinus, Achillea sp.) or two (Myosotis alpestris, Parnassia sp.) middens.

3.3. Midden insects

Insect fossils were recovered from 37 out of 64 middens (Table 2). Coleoptera dominated the midden insect fauna, representing at least 7 families. Of these, ground beetles (Carabidae) were the most diverse with at least 9 taxa, including Amara alpina and Pterostichus (Cryobius) species. Weevils (Curculionidae) occur most frequently with Lepidophorus lineaticollis recovered from 13 samples (max MNI ¼ 4) and Connatichela artemisiae recovered from 9 samples (max MNI ¼ 3). Fly puparia (Diptera) were recovered from 14 samples (max MNI ¼ 4). There were sufﬁcient numbers of ground and rove beetle species to yield Mutual Climatic Range (MCR) estimates of seasonal temperatures. Our estimate of mean July temperature (TMAX) for the MIS 4 assemblages is 10e10.5 C. This is about 5 C colder than modern TMAX at Dawson City (the nearest meteorological station to the study sites). This estimate is similar for Klondike fossil beetle assemblages associated with Dawson tephra and early MIS 2 (Zazula et al., 2006a, 2007). We estimate that mean January temperatures (TMIN) were 16 to 15 C, which is about 10 C warmer than modern TMIN at Dawson City. TMIN MCR estimates are poorly constrained (Elias et al., 1996), but our estimate may still be taken to indicate some degree of winter warming, compared to the modern, highly continental climate of interior Yukon.

4. Interpretations

4.1. Reconstructed paleoenvironments for early MIS 4 in west- central Yukon

Plant macrofossils from the middens provide evidence for the onset of cold, dry conditions and establishment of steppe-tundra vegetation during early MIS 4. Macrofossils indicate this vegetation was rich in graminoids (Elymus sp., Poa sp., Festuca sp., K. myosuroides, Carex spp.), diverse forbs (Thalictrum alpinum, Bupleurum americanum, Draba sp., E. cf. cheiranthoides, Phlox hoodii) and prairie sagebrush (Artemisia frigida). Remains of xerophilous steppe plants, such as A. frigida, P. hoodii, Androsace septentrionalis and Plantago cf. canescens suggest that soils were well-drained and frequently disturbed. The presence of the weevil C. artemisiae provides further evidence for the local abundance of prairie sagebush (A. frigida)ontheearlyMIS4 Fig. 3. Fossil arctic ground squirrel cranium recovered within ice-rich silt underneath landscape. Plants such as Alopecurus sp., Lloydia serotina, Bistorta ice-wedge and Sheep Creek tephra e Klondike. vivipara and T. alpinum are more typical of present-day mesic to well- drained tundra. This vegetation has compositional and functional material (mean RAI mid-point ¼ 50.05, STDV ¼ 33.62). Midden affinities to both present low arctic or alpine well-drained tundra sample sizes vary considerably, with mass ranging from 2.4 to 215 g (Edwards and Armbruster, 1989; Wesser and Armbruster, 1991; (mean ¼ 41.84 g, STDV ¼ 44.93). This wide size range reflects the Walker and Everett, 1991; Lloyd et al., 1994; Walker et al., 2001)and fact that sometimes we were only able to recover partial middens azonal steppe vegetation (Laxton et al.,1996; Vetter, 2000). In terms of from the exposures. Plant macrofossils from the MIS 4 middens the present-day biogeographic affinities of these plants, this vegeta- include at least 45 taxa (Table 1) representing 24 families, domi- tion is best described as a hybrid between steppe and herbaceous nated by forbs (36 taxa), with three kinds of Poaceae (grass), at least tundra, and thus we use the term “steppe-tundra”. two species of dwarf willows (Salix cf. arctica and Salix cf. polaris), Steppe-tundra vegetation probably occupied well-drained, xeric and one tree (Picea spp.; Zazula et al., 2006c; see Figs. 5e7inZazula to mesic substrates on upland habitats developed under cold and et al., 2007). Several taxa were consistently abundant and frequent arid glacial conditions with active loess aggradation (Sanborn et al., in the midden samples (% of samples where taxon present; mean 2006). Since arctic ground squirrels preferably burrow, construct RAI mid-point; maximum RAI), including Poa sp. (84.4%; 8.95; 6), their nests and hibernate about 1 m below the surface (Buck and Draba sp. (75.0%; 11.79; 6), Potentilla sp. (73.4%; 5.01; 4), Salix spp. Barnes, 1999), plant remains within the fossil middens reflects (51.6%; 3.58; 5), Kobresia myosuroides (50.0%; 3.06; 3), and vegetation that occupied former surfaces stratigraphically above G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2225

Fig. 4. a) Lithostratigraphy of MIS 4 deposits at Dominion Creek site showing association of Sheep Creek tephra e Klondike (SCT-K) and Dominion Creek tephra (DC-t) with three distinct generations of ice-wedges and paleosols; b) overview of loess-paleosol stratigraphy at Dominion Creek.

the middens. As such, the midden vegetation data probably reflects assemblages provide evidence for steppe-tundra communities. Even the environment associated with the upper well-drained paleosol though there were fewer MIS 3/2 midden samples (48), they con- (Soil 1), rather than the more mesic conditions suggested by the tained a greater diversity of plant taxa than the larger MIS 4 midden lower paleosols (Soils 2, 3) (Fig. 4; Sanborn et al., 2006). The steppe- record (64 samples); there were at least 60 taxa recovered in the MIS tundra formed a mosaic that also included dwarf willow shrubs in 3/2 middens, while only 45 are present in the MIS 4 samples (Table more mesic microhabitats and rare spruce trees that were probably 1). Some plant taxa recovered within the MIS 3/2 record are confined to sheltered valley bottoms (see Zazula et al., 2006c). conspicuously absent from MIS 4 middens. Interestingly, some taxa The fossil insect assemblages from these samples are similar in that are absent from the MIS 4 samples but present in MIS 3/2 composition, and we treat them here as a single assemblage for the middens are important ecological indicators of alkaline (Suaeda cf. paleoenvironmental reconstruction. Interpretation of a cryoxeric calceoliformis), disturbed (Lappula sp.) or steppe habitats (Anemone steppe-tundra for early MIS 4 based on plant macrofossils is sup- patens var. multifida, Penstemon gormanii). Further, some grasses ported by fossil weevils such as L. lineaticollis and C. artemisiae (Deschampsia ceaspitosa, Alopecurus sp., and Hierochloë hirta ssp. which are well-established members of the MIS 2 fauna from arctica) and other taxa (Conioselinum cnidiifolium,cf.Spiraea beau- Eastern Beringia (Matthews and Telka, 1997; Zazula et al., 2006a, verdiana and Sanguisorba sp.) typically associated with mesic and/or 2007). In addition, there are clear indicators of mesic to moist riparian habitats are also absent in the MIS 4 record. tundra in this fauna, including Pterostichus ventricosus and members of the Cryobius group of the genus Pterostichus. But, the 4.2.1. Multiple Response Permutation Procedure greatest beetle diversity is among taxa associated with dry herba- The MRPP demonstrates that there are highly significant ceous vegetation (A. alpina, Dicheirotrichus cognatus, Harpalus differences between the MIS 4 and MIS 3/2 midden assemblages alaskensis, Harpalus amputatus, and Harpalus opacipennis). The pill (Table 3). The MRPP test statistic is very low (15.6844) with high beetles of the genus Morychus (including Morychus sp. in North significance (P < 0.00001). These results are supported by the America and Morychus viridis in Asia) are additional indicators of apparent pattern of separation of MIS 3/2 and MIS 4 on the scat- steppe-tundra environments in both Eastern and Western Beringia terplot of sites in the NMS ordination (Figs. 5e7). However, the low during the Pleistocene (Elias et al., 2000; Kuzmina and Sher, 2006). MRPP A value (0.03156) indicates that there is high within group M. viridis is an important inhabitant of extant cryoxerophilous heterogeneity in the data. sedge steppe communities in Siberia (Berman, 1990; Berman et al., in this volume). The taxonomic status and ecology of its closest 4.2.2. Indicator Species Analysis relative in Eastern Beringia is less clear, however, because the The ISA demonstrates that some taxa are significantly more species is probably extinct. We can presume that Morychus species abundant and frequent in either the MIS 3/2 or MIS 4 middens in both areas played a similar ecological role during Pleistocene (Table 4). However, the ecological importance of these results may cold stages because they are recorded as fossils synchronously be difficult to assess. There are several significant indicator taxa across Beringia, while becoming virtually extirpated during inter- for MIS 3/2, including Carex sp. (lenticular type), B. vivipara, glacials (Berman, 1990; Berman et al., in this volume). As evidenced Cerastium sp., Stellaria cf. calycantha, and Ranunculus pensylvani- by the midden insect fossils, the environments in the vicinity of the cus-macounii type. The analysis only revealed Salix spp., B. amer- ground squirrel nests appear to have been a mixture of more mesic icanum and T. alpinum as significant indicators for MIS 4 middens. tundra, perhaps in poorly drained valley bottoms, and arid steppe- These species are present during both time intervals and are tundra on better-drained hill slopes. This reconstruction is sup- expected within steppe-tundra vegetation developed under cold, ported by paleobotanical evidence from the squirrel middens. dry Pleistocene conditions. Some possible vegetation differences revealed in our ISA are the significance of Carex spp. (including 4.2. Comparison between Late and Early Wisconsinan midden Carex albo-nigra) remains in MIS 3/2 middens and Salix spp. (dwarf records species including S. cf. polaris and S. cf. arctica) remains during MIS 4. This result may be taken to suggest a greater proportion of Carex Fossil arctic ground squirrel middens from MIS 3/2 and MIS 4 spp. during MIS 3/2 and dwarf willow ground cover at our sites are compositionally different in several ways, although both during early MIS 4. 2226 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Table 1 Plant macrofossil data from MIS 4 and MIS 3/2 middens (after Zazula, 2006, 2007).

Vascular Plants MIS 4 middens MIS 3/2 middens Ecology

Number of Mean RAI Standard Maximum Number of Mean middens mid-point deviation RAI middens RAI mid-point where taxon where taxon present (n,%) present (n,%) Pteropsida Gymnosperma Equiseticaeae Equisetum cf. palustre L. (sheath) n ¼ 0, 0% na na na n ¼ 1, 2.1% 0.01 Wet meadows, lakeshores, woods, shallow waters

Pinaceae Picea sp. (needle) n ¼ 3, 4.7% 0.02 0.11 1 n ¼ 2, 4.2% 0.02 Forests, treeline

Angiosperma Poaceae Deschampsia caespitosa (L.) Beauv, (florets) n ¼ 0, 0% na na na n ¼ 17, 35.4% 1.41 Wet meadows, lakeshores, gravel bars Elymus sp. (floret, spikelet, glumes) incl. n ¼ 28, 43.8% 0.41 0.80 2 n ¼ 29, 60.4% 0.83 Open slopes, well-drained, Elymus trachycaulus (Link) Gould ex Shinners riverbanks Festuca sp. (floret, spikelets) n ¼ 15, 23.4% 0.56 2.12 3 n ¼ 17, 35.4% 0.93 Sandy, gravelly, tundra, open slopes, dunes, lakeshores, woodlands Hierchloë hirta (Schrank) Borba ssp. n ¼ 0, 0% na na na n ¼ 6, 12.5% 0.11 Sandy stream banks, arctica G. Weim (florets, spikelets) lakeshores, meadows Alopecurus sp. (floret) n ¼ 0, 0% na na na n ¼ 7, 14.6% 0.45 Shallow ponds, wet meadows Poa sp. (floret, spikelets) n ¼ 54, 84.4% 8.95 19.04 6 n ¼ 42, 87.5% 7.28 Open slopes, tundra, stream banks

Cyperaceae Carex sp. (lenticular achene) n ¼ 14, 21.9% 0.43 2.05 3 n ¼ 42, 87.5% 4.43 Moist, stream sides, shorelines, meadows Carex sp. (trigonous achenes) n ¼ 4, 6.3% 0.07 0.39 2 n ¼ 8, 16.7% 0.19 Moist, stream sides, shorelines, meadows Kobresia myosuroides (Vill.) Fiori & Paol. n ¼ 32, 50.0% 3.06 5.71 3 n ¼ 23, 47.9% 3.13 Dry locations, calcareous, (achenes, spike fragments) heath, ridges

Juncaeae Juncus sp. (seeds, capsules) n ¼ 1, 1.6% 0.01 0.06 1 n ¼ 5, 10.4% 0.43 Wet meadows, arctic-alpine, river ﬂats, borders of ponds, lakes, streams

Liliaceae Llyodia serotina (L.) Rchb. n ¼ 3, 4.7% 0.02 0.11 1 n ¼ 2, 4.2% 0.02 alpine tundra, rocky, polygonal ground, heaths

Salicaceae Salix sp. (capsules, buds, twigs, n ¼ 33, 51.6% 3.58 9.76 5 n ¼ 17, 35.4% 0.92 leaf fragments) incl. S. polaris, S. arctica Salix cf. arctica Pall. aaaaaa Dry tundra, heath, sedge meadows Salix cf. polaris Wahlenb. aaaaaa Not too dry tundra, late snowbeds, scree slopes

Polygonaceae Bistorta vivipara (L.) n ¼ 10, 15.6% 1.79 6.04 4 n ¼ 30, 62.5% 7.06 Turfy, rocky, moist grassy Delarbre (bulbils) herbmats, manured places Rumex acetosa L. (achenes, calyx) n ¼ 0, 0% na na na n ¼ 3, 6.3% 0.03 Moist alpine or subalpine meadows

Chenopodiaceae Chenopodium sp. (seeds) n ¼ 3, 4.7% 0.06 0.38 2 n ¼ 1, 2.1% 0.01 Disturbed situations, often halophytic Suaeda cf. calceoliformis n ¼ 0, 0% na na na n ¼ 8, 16.7% 0.14 Alkaline ﬂats (Hook.) Moq. (seeds, bracts)

Caryophyllaceae Cerastium sp. (seeds, capsules) n ¼ 16, 25.0% 1.15 5.14 3 n ¼ 29, 60.4% 1.15 Rocky, gravelly or sandy, alpine tundra to heath to meadows Minuartia sp. (seeds) n ¼ 5, 7.8% 0.04 0.14 1 n ¼ 3, 6.3% 0.14 Alpine tundra, snowbeds, gravelly, dry open slopes Silene involucrata (Cham.&Schlecht.) n ¼ 5, 7.8% 0.32 2.03 3 n ¼ 2, 4.2% 0.02 Stony, gravelly, Bocquet (seeds, capsules) river terraces Silene taimyrensis (Tolmatchev) n ¼ 26, 40.6% 2.25 4.96 3 n ¼ 28, 58.3% 1.83 Sandy and rocky open Bocquet (seeds, capsules) slopes and cliffs Silene uralensis (Rupr.) Boquet (seeds) n ¼ 0, 0% na na na n ¼ 2, 4.2% 0.02 Moist alpine slopes and meadows, dunes, seepages G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2227

Table 1 (continued )

Vascular Plants MIS 4 middens MIS 3/2 middens Ecology

Number of Mean RAI Standard Maximum Number of Mean middens mid-point deviation RAI middens RAI mid-point where taxon where taxon present (n,%) present (n,%) Stellaria cf. calycantha (Ledeb.) n ¼ 9, 14.1% 0.07 0.18 1 n ¼ 18, 37.5% 0.34 Alpine tundra, meadows, Bong. (seeds, capsules) riverbanks, dry slopes

Ranunculaceae Anemone narcissﬂora L. s.l. n ¼ 0, 0% na na na n ¼ 6, 12.5% 0.06 Woods and heaths to tundra (winged achenes) Anemone patens var. n ¼ 0, 0% na na na n ¼ 2, 4.2% 0.43 Sandy well-drained multiﬁda Pritzel, L. (achenes) Ranunculus eschscholtzii-sulphureus n ¼ 29, 45.3% 1.06 2.26 3 n ¼ 38, 79.2% 4.35 Moist alpine type (achenes) meadows, herbmats Ranunculus pensylvanicus-macounii n ¼ 3, 4.7% 0.27 2.00 3 n ¼ 29, 60.4% 6.74 type (achenes) Thalictrum alpinum L. (achenes) n ¼ 12, 18.8% 0.73 2.86 3 n ¼ 2, 4.2% 0.07 Alpine herbmats

Papaveraceae Papaver sp. (seeds, capsules) incl. n ¼ 7, 10.9% 0.78 3.40 3 n ¼ 15, 31.3% 1.88 Gravelly sandy soil, Papaver mcconnellii Hultén tundra (and Papaver keelei A.E. Porsild only in MIS 4)

Brassicaceae Draba sp. (seeds, silicles) incl. n ¼ 48, 75.0% 11.79 20.80 6 n ¼ 34, 70.8% 8.82 Calcareous rocky Draba cinerea Adams, barrens and sunny Draba ﬂadnizensis Wulfen cliffs, rocky, gravelly alpine slopes Erysimum cf. cheiranthoides L. n ¼ 28, 43.8% 11.63 25.19 6 n ¼ 24, 50.0% 8.54 Moist turfy places, (seeds, siliques) disturbed situations, lakeshores, creek banks Eutrema edwardsii R. Br. (seeds) n ¼ 4, 6.3% 0.11 0.53 2 n ¼ 8, 16.7% 0.97 Not too dry tundra, heath, calciphile Lepidium densiﬂorum Schrad.(seeds, silicles) na na na na n ¼ 10, 20.8% 1.18 Dry open, disturbed soils

Saxifragaceae Parnassia sp. (seeds) n ¼ 2, 3.1% 0.02 0.09 1 n ¼ 12, 25.0% 0.50 Moist meadows, along streams, lakeshores Saxifraga cf. razshivinii Zhmylev (seeds) n ¼ 1, 1.6% 0.05 0.38 2 n ¼ 7, 14.6% 0.13 Gravelly, rocky, alpine, turfy tundra, herbmats, often calcareous

Rosaceae Potentilla sp. not Potentilla palustris, n ¼ 47, 73.4% 5.01 10.02 4 n ¼ 38, 79.2% 3.93 Gravelly, sandy, open Potentilla norvegica, Potentilla fruiticosa slopes, alpine tundra (achenes, aggregate) Sanguisorba sp. (winged achenes) n ¼ 0, 0% na na na n ¼ 9, 18.8% 0.15 Riverbanks to alpine slopes cf. Spiraea beauverdiana Scneid. n ¼ 0, 0% na na na n ¼ 1, 2.1% 0.01 Borders of muskeg, (seeds, follicles) alpine and subalpine meadows and dry slopes

Fabaceae Astragalus alpinus L. (seed, legume) n ¼ 1, 1.6% 0.01 0.06 1 na na Grassy slopes, heath, moraine, riverbeds Astragalus eucosmus Robins. (seeds, legumes) n ¼ 14, 21.9% 1.58 5.76 4 n ¼ 13, 27.1% 0.14 Gravelly, stony slopes, meadows

Apiaceae Bupleurum americanum Coult. & Rose (carpels) n ¼ 14, 21.9% 1.36 4.31 3 n ¼ 4, 8.3% 0.42 Alpine meadows, moist sand, gravel, scree Conioselinum cnidiifolium (Turcz.) n ¼ 0, 0% na na na n ¼ 6, 12.5% 0.39 Sandy riverbanks, A.E. Porsild (carpels) gravelly slopes, wet meadows.

Primulaceae Androsace septentrionalis L. (seeds, capsules) n ¼ 22, 34.4% 0.61 2.11 3 n ¼ 17, 35.4% 1.03 Dry calcareous, gravelly, disturbed

Gentianaceae Gentiana cf. algida Pall. (seeds, capsules) n ¼ 7, 10.9% 0.34 2.03 3 n ¼ 13, 27.1% 0.67 Alpine meadow, tundra, heath, calcareou. Gentiana cf. prostrata Haenke n ¼ 14, 21.9% 1.48 8.09 5 n ¼ 20, 41.7% 0.90 Moist arctic or (seeds, capsules) alpine tundra, meadows, banks of streams or lakes Gentianella type (seeds, capsules) n ¼ 8, 12.5% 0.42 2.08 3 n ¼ 6, 12.5% 0.06 Tundra slopes, heath, stream banks

(continued on next page) 2228 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Table 1 (continued )

Vascular Plants MIS 4 middens MIS 3/2 middens Ecology

Number of Mean RAI Standard Maximum Number of Mean middens mid-point deviation RAI middens RAI mid-point where taxon where taxon present (n,%) present (n,%) Polemoniaceae Phlox hoodii Richards. (seeds, capsules, leaves) n ¼ 28, 43.8% 0.70 2.12 3 n ¼ 19, 39.6% 0.30 Dry prairies and foothills Polemonium sp. (seeds, capsules) n ¼ 8, 12.5% 0.59 2.82 3 n ¼ 13, 27.1% 1.61 Moist humus, alpine meadows, tundra turf, sand dunes, grassy slopes

Boraginaceae Lappula cf. anisacantha (Turcz. ex Bunge) n ¼ 0, 0% na na na n ¼ 5, 10.4% 0.16 Dry, disturbed habitats Guerke. (nutlets) Mertensia sp. (nutlets) n ¼ 0, 0% na na na n ¼ 6, 12.5% 0.06 Woodlands to tundra, riverbanks Myosotis alpestris Schm. (nutlets) n ¼ 2, 3.1% 0.02 0.09 1 n ¼ 12, 25.0% 0.33 Moist tundra, late snow patches, sandy banks

Scrophulariaceae Castilleja sp. (seeds, capsules) n ¼ 0, 0% na na na n ¼ 2, 4.2% 0.07 Upland tundra, stony slopes, meadows, heath, riverbanks Pedicularis cf. lapponica (seeds, capsule) n ¼ 3, 4.7% 0.02 0.11 1 n ¼ 8, 16.7% 0.62 Dry to moist tundra, heath, calcareous Penstemon gormanii Greene n ¼ 0, 0% na na na n ¼ 8, 16.7% 0.08 Dry, gravelly, disturbed soils (capsule whole, seeds)

Plantaginaceae Plantago cf. canescens Adams (seeds, capsules) n ¼ 14, 21.9% 0.75 2.86 3 n ¼ 15, 31.3% 1.45 Alkaline meadows

Asteraceae Aster/Erigeron type (achenes) n ¼ 6, 9.4% 0.05 0.15 1 n ¼ 6, 12.5% 0.17 Slopes, meadows, river ﬂats, open areas Achillea sp. (achenes) n ¼ 1, 1.6% 0.01 0.06 1 n ¼ 2, 4.2% 0.02 Artemisia frigida Willd. (ﬂowers, leaves) n ¼ 23, 35.9% 1.87 11.13 6 n ¼ 18, 37.5% 0.51 Steep open slopes, dry, disturbed Hieracium type (achenes) n ¼ 0, 0% na na na n ¼ 11, 22.9% 0.49 Alpine meadows, open areas Taraxacum ceratophorum (Ledeb.) DC. s.l. n ¼ 23, 35.9% 2.66 9.57 3 n ¼ 28, 58.3% 1.56 Woodland and (achenes, clusters) heath to tundra

Miscellaneous vegetation n ¼ 64, 100% 50.05 33.62 6 n ¼ 48, 100% 47.25 Mostly graminoid (nesting material) leaves, stems na ¼ no data available (taxon not present). a Present but not quantiﬁed.

4.2.3. Non-metric Multidimensional Scaling with large amounts of Draba sp. (r ¼0.493; r2 ¼ 0.243) and The NMS identified a three dimensional optimal solution (Figs. Ranunculus pensylvanicus-macounii type (r ¼ 0.425; r2 ¼ 0.181) 5e7). The solution is strong as the correlations (r2) between the from those with high amounts of E. cf. cheiranthoides (r ¼ 0.686; distances in the final solution and the distances in the n-dimen- r2 ¼ 0.471) (Fig. 7). The separation of significant indicator taxa is sional species space are 0.272, 0.183, and 0.246 for the first, second also most apparent on Axis 3, where the MIS 4 indicators (Salix and third axes, respectively. This gives a cumulative r2 of 0.702, spp., T. alpinum, and B. americanum) cluster distinctly from MIS 3/2 indicating that most of the variance structuring the dataset has indicators (e.g., B. vivipara, Ranunculus pensylvanicus-macounii been accounted for. In general, there is a large amount of overlap type, and Deschampsia caespitosa). The separation of indicator between samples of the two time intervals, which is especially species from each time interval in ordination space supports the evident between Axis 1 and 2 (Fig. 5) but some samples from each MRPP result of significant differences between the MIS 3/2 and time interval show clear differences. However, according to the MIS 4 midden assemblages. analysis, samples from MIS 3/2 separate well from the MIS 4 samples in species space along all three axes. Axis 1 appears to 5. Discussion separate samples with large amounts of Cerastium sp. (r ¼0.574; r2 ¼ 0.329), S. taimyrensis (r ¼0.524; r2 ¼ 0.274), and Ranunculus 5.1. The Early Wisconsinan (MIS 4) glacial environments of Beringia eschscholtzii-sulphureus type (r ¼0.416; r2 ¼ 0.173) from those with large amounts of E. cf. cheiranthoides (r ¼0.560; r2 ¼ 0.313). MIS 4 or the Early Wisconsinan cold stage (w 90e56 ka) is Because Cerastium sp. and Ranunculus eschscholtzii-sulphureus type recorded in d18O marine records as a time of pronounced Northern are significant indicators for MIS 3/2 taxa, Axis 1 seems to separate Hemisphere glaciation and global sea-level fall, although of lesser samples from the two time intervals (Fig. 5). Axis 2 appears to magnitude than MIS 2 (Martinson et al., 1987). However, local ice separate middens with large amounts of Draba sp. (r ¼ 0.695; advances were more extensive during MIS 4 than MIS 2 in many r2 ¼ 0.483) from the rest of the dataset. Since Draba sp. is abun- areas of Beringia, including; Chukotka Peninsula (Brigham-Grette, dant and frequent in middens from both time intervals, and is not 2001), Seward Peninsula (Kaufman et al., 1996), southwest Alaska a significant indicator taxon, it is difficult to assess the ecological (Kaufman et al., 2001), western Alaska Range (Briner et al., 2005); meaning of Axis 2 (Fig. 6). Axis 3 appears to separate middens Yukon Tanana Upland, (Weber, 1986; Briner et al., 2005) the Brooks G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2229

Table 2 Insects recovered from MIS 4 middens.

Taxon Number of middens Maximum MNI per Ecology where taxon is present midden Ord. Coleoptera Fam. Carabidae Bembidion sp.? 1 1 Mostly riparian species P. (Cryobius) ventricosus Esch. 1 1 On both forest and tundra up to the High Arctic; in forest on riverbanks under leaves, on tundra on moist soil Pterostichus (Cryobius) sp. 1 1 Mostly on moist tundra; in forest on open boggy places and riverbanks Pterostichus (Cryobius) sp.? 1 1 Amara alpina Payk. 5 2 Mostly on dry tundra among herbaceous vegetation; in taiga near tree limit on meadow. One of the most common tundra species today Dicheirotrichus (Trichocellus) cognatus Gyll. 1 1 Circumpolar, mostly in forest, but may occur in coastal tundra, on open, dry places, sandy soil with sparse vegetation Harpalus alaskensis Lth 1 1 On dry tundra with sandy slopes and sparse herbaceous vegetation with Artemisia H. (Harpalomerus) amputatus Say 1 2 Found south of the tundra, on dry sandy grassland Harpalus opacipennis Hald 1 2 Found south of the tundra, on rather dry ground with sparse vegetation Carabidae indet 2 2

Fam. Staphylinidae Olophrum consimile Gyll.? 1 1 Widely distributed Holarctic riparian species, mostly boreal, but single sites also in tundra, in leaf litter (Alnus and Salix) Philonthus duplicatus Bern&Sch. 1 1 Boreal species, live in leaf litter or carrion woods, prey on mycophagous ﬂies

Fam. Scarabaeidae Aphodius albertanus Brown? 1 1 North of North America, boreal

Fam. Byrrhidae Morychus sp. 3 1 Probably an undescribed species associated with tundra-steppe fossil assemblages; most Morychus beetles live today on dry soils with thin moss cover

Fam. Chrysomelidae Chrysolina basilaris (Say) 1 1 Rocky Mountains from Colorado to British Columbia, northern Yukon, common in the Pleistocene steppe-tundra community Galeruca rudis (LeC.) 1 1 From Yukon Territory to California, on lupines

Fam. Curculionidae Lepidophorus lineaticollis Kby 13 4 In tundra on dry sandy soil with poor vegetation, in forest zone on open dry places, common on steppe-like patches. One of the most common Pleistocene beetles in the American Arctic Connatichela artemisiae And. 9 3 In forest zone (Yukon Territory and southern Alaska) on azonal steppe-like slopes, on sandy soil with Artemisia, common in the Late Pleistocene, rare now Connatichela artemisiae And.? 2 1 Vitavitus thulius Kiss.? 1 1 Only on tundra, on dry open ground, common in the Pleistocene, rare now

Fam. Cicadellidae Leafhopper 1 1 In meadows

Ord. Hymenoptera parasitic wasps 4 2

Ord. Lepidoptera Caterpillar 1 1

Ord. Diptera Fly 6 6 Fly puparia 13 4 Indicates rather wet conditions

Insect varia Larvae 1 3 2230 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Table 3 contain loess deposits correlated with the MIS 4 cold stage, though Results of the MRPP testing the null hypothesis of no signiﬁcant difference in paleoecological data are limited (Begét, 2001). Only two Alaskan composition between MIS 3/2 and MIS 4 middens. Average distance is the mean lakes contain sediments with pollen records that extend back to Sørensen’s distance between each pairwise combination of middens from each particular time interval: N is the number of middens samples in each time interval. MIS 4; Imuruk Lake on the Seward Peninsula (Colinvaux, 1964, The observed delta is calculated from the data while the expected delta is derived 1996) and Squirrel Lake in northwest Alaska (Anderson, 1985, from a null distribution; T is the MRPP test statistic, and A is the chance corrected Berger and Anderson, 2000). Both of these lacustrine records ﬁ < within-group agreement. The MRPP was signi cant (P 0.00001). reveal a return to “herb tundra” vegetation following the last Time interval Average distance N MRPP statistics interglacial (MIS 5e). Unfortunately, the limited taxonomic detail MIS 3/2 0.67926 48 Observed delta ¼ 0.69794 and age uncertainties with these two lacustrine records hinder MIS 4 0.71195 64 Expected delta ¼ 0.72068 detailed interpretations about the structure and composition of T ¼15.6844, A ¼ 0.03155, MIS 4 vegetation or how it relates compositionally to MIS 2 P < 0.00001 communities. In central Yukon, new dates on SCt-K (Westgate et al., 2005, Ranges (Hamilton, 1994; Briner et al., 2005) and the St. Elias 2008) indicate that organic-rich silt (loess) overlying Reid glacial mountains of southern Yukon (Ward et al., 2008). The collective deposits at the Ash Bend locality (Hughes et al., 1987; Westgate MIS 4 geologic record suggests that glaciations in Beringia are et al., 2001) records the MIS 5/4 transition. Schweger’s (2003) asynchronous with global ice volume, likely the result of greater pollen record from Ash Bend documents the transition between moisture availability during MIS 4 since lower MIS 2 sea levels may spruce dominated dense boreal forest during the last interglacial have drove Beringian moisture sources much further away from the (MIS 5) to forest-tundra (Zone I), birch shrub tundra (Zone II) and interior (Brigham-Grette, 2001). Regardless of the glacial geologic then herb tundra (Zone III) associated with glacial conditions of record, the aeolian stratigraphic record of loess and sandsheets in early MIS 4. Importantly, pollen-spectra immediately below and the Klondike supports the notion of an arid-continental, full-glacial above the SCt-K contain only 5 and 2% Picea with 18 and 5% Betula, climate during MIS 4 in the interior of Eastern Beringia. respectively, and the assemblages are dominated by Cyperaceae, Little is known about ecosystems of Eastern Beringian during Poaceae, and Artemisia. Thus, in central Yukon during the MIS 5/4 Pleistocene cold stages prior to MIS 2. Several sites in central Alaska transition, pollen data suggests that SCt-K fell on forest-tundra

Fig. 5. NMS ordination of all midden samples and plant taxa on Axis 1 and 2. Blue triangles represent MIS 4 samples. Red triangles represent MIS 3/2 samples. Blue crosses represent plant taxa. Axis 1 appears to separate samples with abundant Cerastium (r ¼0.574; r2 ¼ 0.329), Silene taimyrensis (r ¼0.524; r2 ¼ 0.274), and Ranunculus eschscholtzii- sulphureus type (r ¼0.416; r2 ¼ 1.73) from those with abundant Erysimum cf. cheiranthoides (r ¼ 0.560; r2 ¼ 0.313). Axis 2 appears to separate middens with abundant Draba (r ¼ 0.695; r2 ¼ 0.483) with the rest of the dataset. G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2231

Fig. 6. NMS ordination of all midden samples and plant taxa on Axis 1 and 3. Blue triangles represent MIS 4 samples. Red triangles represent MIS 3/2 samples. Blue crosses represent plant taxa. Axis 1 appears to separate samples with abundant Cerastium (r ¼0.574; r2 ¼ .329), Silene taimyrensis (r ¼0.524; r2 ¼ 0.274), and Ranunculus eschscholtzii- sulphureus type (r ¼0.416; r2 ¼ 1.73) from those with abundant Erysimum cf. cheiranthoides (r ¼ 0.560; r2 ¼ 0.313). Axis 3 appears to separate middens with abundant Draba (r ¼ 0.493; r2 ¼ 0.243) and Ranunculus pensylvanicus-macounii type (r ¼ 0.425; r2 ¼ 0.181) from those with abundant Erysimum cf. cheiranthoides (r ¼ 0.686; r2 ¼ 0.471). The sep- eration of taxa identiﬁes as signiﬁcant in the Indicator Species analysis is most apparent on Axis 3, where the MIS 4 indicators (Salix, Thalictrum alpinum, and Bupleurum americanum) cluster towards the bottom distinctly from MIS 3/2 indicators (e.g. Bistorta vivipara, Ranunculus pensylvanicus-macounii type, and Deschampsia caespitosa) which cluster towards the top.

ecotonal vegetation that may have resembled extant birch shrub vegetation composition or structure (i.e. steppe-tundra). As such, tundra communities near latitudinal treeline (Schweger, 2003). the multivariate results suggest that the midden contents may be This vegetation was replaced by herb or steppe-tundra more typical highly influenced by foraging upon dense concentrations of of full-glacial conditions during early MIS 4. This pollen inferred particular plants that produce relatively large numbers of seeds and moisture gradient at Ash Bend through the MIS 5/4 transition is fruits in close proximity to individual arctic ground squirrel similar to evidence for increasing aridity during this interval based burrows (e.g. E. cf. cheiranthoides, Draba sp., Cerastium sp., Ranun- on loess paleosols in the Klondike (Sanborn et al., 2006). Further, culus spp.). Most of the plant taxa indicative of steppe-tundra the reconstructed steppe-tundra from the Klondike arctic ground vegetation are common between the MIS 3/2 and MIS 4 middens squirrel middens is probably correlative to Schweger’s (2003) herb- (Table 1) as suggested by the high overlap in samples revealed in zone pollen-spectra (Pollen Zone III) from Ash Bend. the NMS (especially Axis 1 and 2 as demonstrated in Fig. 5), though they may differ in frequency and abundance (Zazula et al., 2007). 5.2. Steppe-tundra during two successive Late Pleistocene glacial Plant taxa shared between the two time intervals include grami- intervals noids (Elymus sp., Poa sp., Festuca sp., K. myosuroides), prairie sagebrush (A. frigida), diverse forbs (Draba sp., E. cf. cheiranthoides, Although our multivariate analyses indicate that floristic Potentilla sp., S. taimyrensis, P. cf. canescens, P. hoodii), dwarf shrubs composition of MIS 3/2 middens differ statistically from those of (S. cf. polaris, S. cf. arctica) and rare conifers (Picea spp.). The co- MIS 4, these distinctions may not be very important for the overall occurrence of many of the important steppe-tundra indicator paleoenvironmental reconstruction. Differences revealed by our plants suggests that that vegetation was probably compositionally multivariate analyses of plant remains are more likely the result of and structurally similar during the onset of both major glacial minor differences in cache foraging activity in relation to site intervals of the Late Pleistocene. This overall similarity is consistent specific differences in vegetation (see Gillis et al., 2005a; Zazula with evidence from loessal paleosols (Sanborn et al., 2006) and et al., 2006b), rather than substantial differences in zonal insect faunas which are dominated by L. lineaticollis and C. 2232 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Fig. 7. NMS ordination of all midden samples and plant taxa on Axis 2 and 3. Blue triangles represent MIS 4 samples. Red triangles represent MIS 3/2 samples. Blue crosses represent plant taxa. Axis 2 appears to separate middens with abundant Draba (r ¼ 0.695; r2 ¼ 0.483) with the rest of the dataset. Axis 3 appears to separate middens with abundant Draba (r ¼ 0.493; r2 ¼ 0.243) and Ranunculus pensylvanicus-macounii type (r ¼ 0.425; r2 ¼ 0.181) from those with abundant Erysimum cf. cheiranthoides (r ¼ 0.686; r2 ¼ 0.471). The separation of taxa identiﬁes as signiﬁcant in the Indicator Species Analysis is most apparent on Axis 3, where the MIS 4 indicators (Salix, Thalictrum alpinum, and Bupleurum americanum) cluster towards the bottom distinctly from MIS 3/2 indicators (e.g. Bistorta vivipara, Ranunculus pensylvanicus-macounii type, and Deschampsia caespitosa) which cluster towards the top. artemisiae. MCR paleotemperature reconstructions for MIS 3/2 present, for most (w80%) of the Pleistocene (Ehlers and Gibbard, (Zazula et al. 2006a) and MIS 4 suggest that growing season 2004). As such, glacial or interstadial conditions associated with temperatures were similar, characterized by reductions of about Pleistocene cold intervals are considered to represent the climatic 5 C. The growth of extensive glaciers in the northern Cordillera “norm” for many organisms, while interglacial conditions, such as during MIS 4 and MIS 2 would have resulted in a reduction of the Holocene epoch, may be viewed as temporary “disturbances” moisture sources and increased continentality in the interior of that glacial-adapted organisms endured by migrating to suitable Alaska and Yukon. habitats (Rull, 2009). During the most recent glacial cycle, species that could not endure the transition to the present interglacial by 5.3. Glacial and interglacial refugia establishing themselves within interglacial refugia became extinct or locally extirpated. Much research in Beringia has focused on the concept of “glacial Beringia was a glacial refugium for arctic species during Pleis- refugia” with aim to reconstruct the composition of past commu- tocene cold periods when much of northern North America was nities and distribution of arctic species during the most recent covered by continental ice (Hultèn, 1937; Hopkins et al., 1982). Pleistocene cold stage (Hopkins et al., 1982). A recent synthesis of Conversely, small, disjunct habitats within the zonal environment refugia theory by Rull (2009) provides a critical distinction between of present-day Beringia serve as interglacial refugia for glacial- the concepts of glacial refugia and “interglacial refugia”. This adapted species. These interglacial refugia in Beringia are generally distinction is rooted in the notion that the Earth has been effected characterized as “microrefugia”, which are often small diffuse areas by glaciation, or at least interstadial conditions that are colder than and result in highly fragmented populations for many glacial- G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2233

Table 4 Indicator and randomized indicator values for species that are signiﬁcant (P < 0.05) indicators of one of the two time intervals in the midden dataset.

Time interval Species Indicator value Randomized P-value indicator value MIS 3/2 (w24e2914C ka BP) Carex sp. (lenticular achenes) 76.7 29.6 0.0010 Bistorta vivipara 48.9 22.2 0.0010 Cerastium sp. 40.5 24.5 0.0030 Ranunculus 54.0 34.3 0.0010 eschscholtzii-sulphureus type Ranunculus 58.5 18.3 0.0010 pensylvanicus-macounii type Deschampsia caespitosa 35.4 10.8 0.0010 Stellaria cf. calycantha 26.9 15.9 0.0100 Parnassia sp. 23.8 9.4 0.0010 Myosotis alpestris 22.8 9.3 0.0010 Hieracium type 22.9 7.9 0.0010 Lepidium densiﬂorum 20.8 7.2 0.0010 Papaver sp. 21.8 13.4 0.0070

MIS 4 (w82 kyr) Salix spp. (dwarf) 36.1 27.1 0.0300 Thalictrum alpinum 16.5 9.4 0.0190 Bupleurum americanum 17.0 11.5 0.0410

adapted arctic and alpine species. Interglacial refugia represent at aspects of the mammoth-steppe may have responded to Quater- least partial structural and functional analogues to conditions that nary climatic-environmental oscillations in Beringia. In particular, were formerly widespread and continuous across the former there are three critical aspects of arctic ground squirrel ecology that habitat range for these species during glacial intervals. A good must be considered in this discussion. Firstly, the present distri- example is the arctic/alpine dwarf shrub Dryas octopetala which has bution of arctic ground squirrels is largely determined by the populations that are highly fragmented as a result of enduring presence of permafrost because they cannot burrow into frozen numerous glacial and interglacial cycles, a complex post-glacial soils and require well-drained substrates suitable for burrowing, history and reliance on specific microhabitats (Max et al., 1999; nesting and successful hibernation. As such, they tend to establish Skrede et al., 2006). Rull’s concept of interglacial refugia for arctic their colonies in well-drained areas of alpine or arctic tundra, or organisms that are adapted to glacial conditions provides a valuable dry, open meadows (Fig. 8; Bee and Hall, 1956; Carl, 1971; Nadler framework for reconstructing past glacial environments in Beringia and Hoffmann, 1977; McLean, 1985; Buck and Barnes, 1999; Gillis and for understanding present-day biogeographic patterns of et al., 2005a,b). Secondly, arctic ground squirrels are at less risk of steppe-tundra vegetation, and associated fauna such as arctic predation in open habitats (e.g. tundra or steppe-tundra) with ground squirrels. minimal visual obstruction because they require a clear line of site to detect predators and escape to their burrow for protection 5.4. Arctic ground squirrel adaptations (Karels and Boonstra,1999; Hik et al., 2001; Gillis et al., 2005b). This risk of predation resulting from vegetation cover has important fi This squirrel is best adapted to carry on the life processes of feeding, implications for overall population tness for arctic ground squir- hibernating and evading enemies in areas where permafrost is rels (Hik et al., 2001). Thirdly, arctic ground squirrels can subsist on several feet below the surface of the ground (Bee and Hall,1956: 47). Present-day arctic ground squirrel populations range in distribution from northeast Siberia across mainland northern North America to Hudson Bay (Figs. 8 and 9; Nadler and Hoffmann, 1977). However, within this geographic range, their populations are highly fragmented, and largely confined to well-drained alpine and arctic tundra or open areas within the boreal forest (Fig. 8). This patchy distribution and restriction to suitable azonal habitats indicates that the species is confined at present within interglacial refugia. There is a conspicuous absence of arctic ground squirrels in the dense boreal forest of interior Alaska and Yukon at present (Nadler and Hoffmann, 1977; Kurtén and Anderson, 1980; Fig. 9). This zone of absence separates the northern populations (S. parryii ssp. parryii) from the southern clade (Spermophilus parryii plesius) and is likely the result of Quaternary biogeographical range disruptions (Eddingsaas et al., 2004), rather than the complete lack of suitable habitat, because this zone does contain alpine ecosystems and open areas within the boreal forest. In contrast, the fossil midden record indicates that arctic ground squirrel populations were much more widespread and abundant throughout the interior of Alaska and Yukon during Late Pleistocene glacial intervals, extending well beyond their modern Fig. 8. Southwest facing slope with steppe vegetation, well-drained loessal soil and arctic ground squirrel colony in the boreal forest of southwest Yukon near Kluane Lake. interglacial range, (Harington, 2003; Zazula et al., 2005, 2007). These habitats are disjunctly dispersed within the boreal forest of southern Yukon and The present-day ecology and distribution of arctic ground may be considered interglacial refugia for some organisms that were more widespread in squirrels is informative to address how this species and some other Beringia during Pleistocene cold intervals (Laxton et al.,1996; Zazula et al., 2006b, 2007). 2234 G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237

Fig. 9. Maps of Beringia demonstrating glacial vs. interglacial ranges for arctic ground squirrels in Beringia. A) Glacial Beringia. The green area is the ice free landscape that may have served as habitat for arctic ground squirrels during Pleistocene glacial conditions. Note the presence of Pleistocene arctic ground squirrels at sites near Dawson City (Klondike) and Fairbanks where they are absent at present. B) Interglacial range for arctic ground squirrels as demonstrated by their modern distribution in green (present distribution after Nadler and Hoffmann, 1977). Note the present-day absence of arctic ground squirrels in the interior of Alaska and Yukon, including Dawson City (Klondike) and Fairbanks.

a wide variety of cache food items in both boreal and tundra 5.4.2. Arctic ground squirrel responses to past environmental habitats and develop habitat or site speciﬁc cache foraging strate- change gies (Gillis et al., 2005a,b; Zazula et al., 2006b). Paleoecological records indicate that past interglacial boreal forests in central Alaska and Yukon were similar in composition 5.4.1. Arctic ground squirrels of the mammoth-steppe and structure to those of today (e.g. MIS 5; Muhs et al., 2001, Arctic ground squirrels have a long history in Beringia and have Hamilton and Brigham-Grette, 1991; Péwé et al., 1997; Schweger persisted through repeated glacialeinterglacial cycles (Eddingsaas et al., in this volume). Closed boreal forests with shallow perma- et al., 2004). Fossil evidence (Storer, 2003) indicates that arctic frost and visually obstructive vegetation are important factors that ground squirrels have been present in Yukon since the Early prevent the establishment of arctic ground squirrels in much of the Pleistocene (>740 000 yr), arriving in Eastern Beringia after interior today, and it is reasonable to assume that they were also divergence from ancestral Siberian populations (Nadler and locally rare or extirpated during the last interglacial (MIS 5). Hoffmann, 1977). Divergence estimates based on mitochondrial However, arctic ground squirrel populations were able to track the DNA mutation rates (Eddingsaas et al., 2004)suggestasplit establishment of interglacial forests in the interior and migrate to occurred in North America between the northern and southern disjunct interglacial microrefugia (Rull, 2009) that retained char- subspecies between 940 000 and 790 000 yr ago. Further diver- acteristics of the formerly widespread glacial mammoth-steppe gence into the four geographically distinct clades occurred at the (Fig. 8). Interglacial microrefugia for steppe-tundra organisms onset of major cold stages of the Middle and Late Pleistocene. include dry alpine tundra (Edwards and Armbruster, 1989; Wesser Since w80% of the Quaternary can be characterized by glacial, or at and Armbruster,1991; Lloyd et al.,1994; Gillis et al., 2005b), south- least interstadial conditions, environmental conditions of the facing steppe-dominated slopes and meadows (Fig. 8; Laxton et al., mammoth-steppe can be considered the ecological “norm” for 1996; Vetter, 2000; Guthrie, 2001) and well-drained sites in Arctic arctic ground squirrels. tundra (Carl, 1971; Walker and Everett, 1991; Walker et al., 2001). The fossil midden record provides clear evidence for the asso- Given that only w20% of Quaternary is characterized by non- ciation of arctic ground squirrels, steppe-tundra vegetation, well- glacial conditions (Ehlers and Gibbard, 2004), interglacials in drained loessal soils, and cryoxeric climates e all key ecological Beringia can be seen as temporary disturbance intervals in the characteristics of the mammoth-steppe biome as envisioned by evolutionary history of arctic ground squirrels, steppe-tundra Guthrie (1990, 2001). Analysis of middens from two time periods vegetation and other organisms that are adapted to cold, dry indicate that the mammoth-steppe was successfully established glacial environments. during the last two major cold stages of the Late Pleistocene. Based Conversely, as climates cooled following the last interglacial on these data, we can reasonably extrapolate that the mammoth- (MIS 5/4 transition), ice sheets expanded and the continental steppe, complete with loess deposition, steppe-tundra expansion, interior of Alaska and Yukon became more arid with widespread, widespread colonization of arctic ground squirrels, and establish- active loess deposition. The return to glacial conditions created ment of megafaunal grazing communities also accompanied earlier nearly continuous, zonal habitat across much of Beringia for arctic Pleistocene cold stages in Beringia. ground squirrels and other glacial-adapted species in places such as G.D. Zazula et al. / Quaternary Science Reviews 30 (2011) 2220e2237 2235

Fairbanks and the Klondike (Fig. 9). Our midden data suggests that Acknowledgements the MIS 5 interglacial boreal forests in the interior were replaced by open steppe-tundra vegetation that expanded from disjunct This work was made possible with the support of the Klondike interglacial microrefugia. Arctic ground squirrel populations placer mining community, including Jim, Dagmar, Tara and Seamus tracked the expansion of steppe-tundra habitats from disjunct Christie, Bernard and Ron Johnson, Stuart Schmidt, and Ken Tatlow. interglacial refugia back into the interior during the MIS 5/4 tran- Funding was provided by grants from the Geological Society of sition and established widespread populations on the mammoth- America, Northern Scientific Training Program of DIAND, and a Sir steppe. The expansion of arctic ground squirrel populations likely James Lougheed Scholarship to Zazula. Mathewes and Froese were had important implications for genetic mixing and high rates of funded by NSERC Discovery grants. The fossil insect research for gene flow as formerly isolated interglacial populations became this project was funded by a grant to Elias by the Leverhulme trust, reunited during subsequent cold stages (Eddingsaas et al., 2004). F/07 537/T. Alice Telka (Paleotec Ltd.), Bruce Bennett (Yukon The widespread establishment of arctic ground squirrels during Renewable Resources), Carolyn Parker and David Murray (Univer- Quaternary cold stages in Beringia suggests they are ideally adapted sity of Alaska Herbarium) helped with the identification of some to glacial conditions and have an evolutionary history linked to the plant macrofossils. We thank the University of British Columbia, mammoth-steppe (Eddingsaas et al., 2004). A hallmark character- University of Alaska, Fairbanks and University of Alberta herbar- istic of arctic ground squirrels has been their ability to endure the iums for allowing us to examine and sample reference plant numerous climate driven expansions and retractions of the specimens. We thank Alberto Reyes, Paul Sanborn, Scott Smith, mammoth-steppe by tracking environmental changes and estab- Elizabeth Hall, Victoria Castillo, Charles Schweger, John Westgate, lishing populations in diffuse interglacial refugia during relatively Brent Alloway, Alan Cooper and Eske Willerslev for assistance and brief Quaternary warm intervals. The ability to subsist on a wide companionship in the field. Brent Ward, Alton Harestad and Eliz- variety of plants may be a key factor that enabled arctic ground abeth Elle assisted with earlier drafts of this paper. We are thankful squirrel populations to track these environmental fluctuations, for helpful reviews by Scott Armbruster, Tom Ager and Mary disperse to new, sometimes sub-optimal, habitats, and maintain Edwards which substantially improved the manuscript. This paper viable populations over glacial-interglacial time scales. Present-day is dedicated to the memories of Dick Morlan and Andrei Sher interglacial microrefugia that include thriving arctic ground whose passion for Beringia left us with a legacy of innovative and squirrel populations with well-drained soils, and steppe and/or inspirational research. herbaceous tundra vegetation should be considered at least partial relict habitats of the former glacial mammoth-steppe biome and References further investigated to provide information on Pleistocene ecosystems of Beringia. Ager, T.A., 2003. Quaternary vegetation and climate history of the central Bering land bridge from St. Michael Island, western Alaska. 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